New maximum likelihood estimators for eukaryotic intron evolution

Abstract

The evolution of spliceosomal introns remains poorly understood. Although many approaches have been used to infer intron evolution from the patterns of intron position conservation, the results to date have been contradictory. In this paper, we address the problem using a novel maximum likelihood method, which allows estimation of the frequency of intron insertion target sites, together with the rates of intron gain and loss. We analyzed the pattern of 10,044 introns (7,221 intron positions) in the conserved regions of 684 sets of orthologs from seven eukaryotes. We determined that there is an average of one target site per 11.86 base pairs (bp) (95% confidence interval, 9.27 to 14.39 bp). In addition, our results showed that: (i) overall intron gains are approximately 25% greater than intron losses, although specific patterns vary with time and lineage; (ii) parallel gains account for approximately 18.5% of shared intron positions; and (iii) reacquisition following loss accounts for approximately 0.5% of all intron positions. Our results should assist in resolving the long-standing problem of inferring the evolution of spliceosomal introns.

Figure 1. Two Hypotheses for the Relationship among Three Groups: Arthropods (A), Nematodes (N), and Deuterostomes (D)

The coelomata hypothesis is shown on the left, and the ecdysozoa hypothesis is shown on the right.

Figure 2. Relationship between θ and the Maximum Log-Likelihood Value

The ecdysozoa phylogeny was used. The maximum log-likelihood value was calculated by treating all parameters other than θ as nuisance parameters and maximizing over them. The arrow shows the MLE of θ as 0.071. The horizontal line indicates a 95% CI of 0.055–0.096. The maximum log-likelihood value at the MLE of θ was −255.48.

Figure 3. MLEs of the Number of Gains and Losses Using the Ecdysozoa Phylogeny

Numbers of introns present in modern species (known) are in black. Numbers of introns present in ancestors (estimated) are in green. Numbers of gains and losses (estimated) are in red and blue, respectively. Branches that experienced >1.5 gains per loss are shown in red, and those that experienced >1.5 losses per gain are in blue. D.mel, D. melanogaster; A.gam, A. gambiae; C.ele, C. elegans; H.sap, H. sapiens; S.pom, S. pombe; A.tha, A. thaliana; P.fal, P. falciparum.

Figure 4. Comparison of Results between the EM algorithm (θ = 100) and a Previous ML Method [6]

The results of the EM algorithm when using θ = 100 are shown. Numbers in parentheses indicate the differences between the two results using our results as the benchmark. Numbers of introns present in modern species (known) are in black. Numbers of introns present in ancestors (estimated) are in green. Numbers of gains and losses (estimated) for each branch are in red and blue, respectively. Branches that experienced >1.5 gains per loss are shown in red, and those that experienced >1.5 losses per gain are in blue. D.mel, D. melanogaster; A.gam, A. gambiae; C.ele, C. elegans; H.sap, H. sapiens; S.pom, S. pombe; A.tha, A. thaliana; P.fal, P. falciparum.